Introduction
North Africa, defined as the southern Mediterranean region or northern Sahara (El Mahrad et al., Reference El Mahrad, Abalansa, Newton, Icely, Snoussi and Kacimi2020), features predominantly arid coastal terrain with sand ridges, lagoons, salt marshes, and alluvial plains, covering over half its landscape (Hzami et al., Reference Hzami, Heggy, Amrouni, Mahé, Maanan and Abdeljaouad2021). The Mediterranean coastlines, spanning 5712 km from Egypt to the Strait of Gibraltar, include Egypt (950 km; Bird, Reference Bird and Bird2003), Libya (1850 km; Schwartz, Reference Schwartz and Bird2010), Tunisia (1200 km; Khiari et al., Reference Khiari, Atoui, Khalil, Charef and Aleya2017), Algeria (1200 km; Bakalem et al., Reference Bakalem, Gillet, Pezy and Dauvin2020), and Morocco (512 km; Er-Ramy, Reference Er-Ramy, Nachite, Anfuso and Williams2022), highlighting significant geographical and environmental diversity (Connah, Reference Connah2015). However, despite this diversity, the marine fauna along the North African Mediterranean coasts remains relatively understudied, particularly in terms of marine annelids. Polychaetes, a class of annelid worms, are integral components of marine ecosystems, playing crucial roles in nutrient cycling, sediment dynamics, and serving as indicators of environmental health (Beesley et al., Reference Beesley, Ross and Glasby2000). Among these, the family Hesionidae Grube, 1850 is characterized by a short, cylindrical and stout body, with generally a small number of chaetigers, marked cephalisation, prostomium without palps and several anterior segments carry long cirri. The members of this family can live in rocky or sandy bottoms and in a wide range of depth, but they are seldom abundant (Rizzo et al., Reference Rizzo and Salazar-Vallejo2014; Salazar-Vallejo, Reference Salazar-Vallejo2018). The Hesionidae was revised by Pleijel (Reference Pleijel1998), and the structure of his classification is followed and used by the world's scientific researchers. This family currently includes over 175 species belonging to 28 genera and several subfamilies (Rouse et al., Reference Rouse, Carvajal and Pleijel2018). Nonetheless, comprehensive surveys and taxonomic assessments of Hesionidae in North African waters are limited. Only two species, Oxydromus flexuosus (Delle Chiaje, 1827) and Pilargis verrucosa Saint-Joseph, 1899, have been particularly reported in Moroccan marine waters (Gillet, Reference Gillet2017). In contrast, 9 species have been identified along the Algerian coastline: Gyptis propinqua Marion & Bobretzky, 1875, Hesione splendida Lamarck, 1818, Leocrates claparedii (Costa in Claparède, 1868), Nereimyra punctata (Müller, 1788), Oxydromus agilis (Ehlers, 1864), O. flexuosus (Delle Chiaje, 1827), Oxydromus pallidus Claparède, 1864, Psamathe fusca Johnston, 1836 and Syllidia armata Quatrefages, 1866 (Bakalem et al., Reference Bakalem, Gillet, Pezy and Dauvin2020). In Tunisian waters, nine species have been documented: H. splendida Lamarck, 1818, Hesionides arenaria Friedrich, 1937, Hesionides gohari Hartmann-Schröder, 1960, Microphthalmus sczelkowii Metschnikow, 1865, Microphthalmus similis Bobretzky, 1870, O. agilis (Ehlers, 1864), O. flexuosus (Delle Chiaje, 1827), P. fusca Johnston, 1836 and S. armata Quatrefages, 1865 (Ayari-Kliti et al., Reference Ayari-Kliti, Bakalem, Fersi, Afli and Dauvin2022). On the Egyptian coasts, 11 species have been recorded: G. propinqua (Marion & Bobretzky, 1875), Hesione pantherina Risso, 1826, H. arenaria Friedrich, 1937, Microphthalmus aberrans (Webster & Benedict, 1887), M. sczelkowii Mecznikow, 1865, Neogyptis mediterranea (Pleijel, 1993), O. agilis (Ehlers, 1864), Oxydromus obscurus (Verrill, 1873), O. pallidus Claparède, 1864, Podarkeopsis capensis (Day, 1963) and S. armata Quatrefages, 1866 (Abd Elnaby, 2009; Dorgham et al., Reference Dorgham, Hamdy, El-Rashidy and Atta2013, Reference Dorgham, Hamdy, El-Rashidy, Atta and Musco2014; Hamdy and Ibrahim, Reference Hamdy and Ibrahim2019; Abd Elnaby, Reference Abd Elnaby2020; Hamdy et al., Reference Hamdy, Elebiary, Abd-Elnaby, Dorgham and Hamdan2023a).
The genus Hesione Savigny in Lamarck, 1818, encompasses specimens characterized by several distinctive features: they typically have 16 chaetigers, 2 antennae that are generally simple (non-articulated), a prostomium lacking palps, 2 pairs of eyes with the anterior pair often larger and more widely spaced compared to the posterior pair, sesquiramous parapodia (featuring dorsal cirri but lacking notochaetae), as well as eight pairs of long anterior cirri and striking pigmentation patterns (Pleijel, Reference Pleijel1998; Salazar-Vallejo, Reference Salazar-Vallejo2018). Hesione was regarded as including a single species, H. pantherina Risso, 1826, which was found in the Atlantic Ocean (specifically along the Basque coast), Mediterranean Sea, Red Sea, and Persian Gulf (Fauvel, Reference Fauvel1923). However, later research by Pleijel (Reference Pleijel1998) suggested that Hesione includes 18 species and concluded that their classification was somewhat unclear and requiring further examination and revision. Recently, Salazar-Vallejo (Reference Salazar-Vallejo2018) conducted a comprehensive revision of the taxonomy of the genus Hesione, expanding it to include a total of 23 species. This revision recognized 12 previously described species as well as 11 newly discovered species. It is worth noting that, till now, there is no published evidence of any Hesione species being found on the Moroccan coasts, except for one specimen of Hesione sicula collected from a depth of 50 m near the Moroccan-Mauritanian borders during the Cruise 36 mission, Sta. 115 in 1975 (Salazar-Vallejo, Reference Salazar-Vallejo2018). This scarcity of investigations may be attributed to the relatively few studies conducted along the Moroccan coasts. Nevertheless, this discovery is significant as it extends the geographical distribution of this genus into one of the world's less explored regions.
Up to this point, there have been no reports of this species in the Mediterranean coastlines of North Africa (Gillet, Reference Gillet2017; Salazar-Vallejo, Reference Salazar-Vallejo2018; Bakalem et al., Reference Bakalem, Gillet, Pezy and Dauvin2020; Ayari-Kliti et al., Reference Ayari-Kliti, Bakalem, Fersi, Afli and Dauvin2022; Abd Elnaby, Reference Abd Elnaby2005; Dorgham et al., Reference Dorgham, Hamdy, El-Rashidy and Atta2013, Reference Dorgham, Hamdy, El-Rashidy, Atta and Musco2014; Hamdy and Ibrahim, Reference Hamdy and Ibrahim2019; Abd Elnaby, Reference Abd Elnaby2020; Abd Elnaby and Abdelsalam, Reference Abd Elnaby and Abdelsalam2021; Rasha et al., Reference Rasha, Noha, Mohamed, Giorgos and Amira2022; Hamdy et al., Reference Hamdy, Elebiary, Abd-Elnaby, Dorgham and Hamdan2023a, Reference Hamdy, Elebiary, Abdel Naby, Borghese, Dorgham, Hamdan and Musco2023b; Abdelsalam and Elebiary, Reference Abdelsalam and Elebiary2023; Elebiary et al., Reference Elebiary, Abd Elnaby, Dorgham, Hamdan and Hamdy2023). Therefore, this paper presents the first documented occurrence of this species along the Mediterranean coasts of North Africa, marking the initial record of the genus Hesione in Moroccan Mediterranean marine waters.
Material and methods
Study area
Amsa Bay (Figure 1) is positioned roughly 18 km east of Tetouan along the Moroccan Mediterranean coastline (35°31′59.5″N, 5°13′29.0″W). Our research focuses on the relevance of suspended longline systems supported by lantern nets as farming structures, at the Amsa Shellfish Research Station. Within these structures, we conducted our experiments with mussel spat of Mytilus galloprovincialis. Each lantern comprised five levels, each with a surface area of 2000 cm2, while the aberture (small squares) of the net had 0.9 cm. These lanterns were suspended at depths ranging from 2.5 to 4 m within the infralittoral belt. Additionally, in-situ measurements of seawater parameters when the species was first recorded, yielded the following results: Temperature = 21.08°C, Salinity = 36.27 psu, and pH = 8.51.
Geographic localization of Amsa Bay and sea farming structure (longline).
Sampling and taxonomic analysis
Macrofauna found in lantern nets associated with mussels (Figure 2) was sampled, for the first time in October 2021, in the infralittoral belt (from 2.5 to 4 m depth) of the Amsa shellfish farm. The sampling process consisted of: (i) collecting lantern nets from the sea, (ii) extracting mussels and their associated fauna from each level of the lantern, and (iii) recovering and conservation of the sampled macrofauna. The associated macrofauna samples were placed in plastic boxes and fixed in an 8% sea-water solution of commercial formaldehyde.
Extraction process of macrofauna. A, Lantern collection from longline; B, mussels and macrofauna extraction; C, lantern rinsing; D, macrofauna captured in a sieve after lantern rinsing.
In the laboratory, macrofauna was rinsed in freshwater, preserved in 70% ethanol and sorted. Polychaetes were identified to species level following Gil (Reference Gil2011) and counted. However, five specimens of Hesione genus were identified following the taxonomic key to species of Hesione Savigny in Lamarck, 1818 prepared by Salazar-Vallejo (Reference Salazar-Vallejo2018), and were subsequently deposited in the Museum of Natural History, Marrakech, under the registration number MHNM 24 ZRP4.
Results
Systematic account
Class Polychaeta Grube, 1850
Subclass Errantia Audouin & Milne-Edwards, 1832
Order Phyllodocida Dales, 1962
Suborder Nereidiformia Glasby, 1993
Family Hesionidae Grube, 1850
Subfamily Hesioninae Grube, 1850
Genus Hesione Savigny in Lamarck, 1818
Hesione sicula delle Chiaje, 1830
(Fig. 3A–I)
Hesione sicula, Salazar-Vallejo, Reference Salazar-Vallejo2018: 301–308, 317, figs 48–51
Material examined
In October 2021, five specimens of H. sicula were initially observed in association with M. galloprovincialis at the Amsa shellfish farm. Subsequently, an additional five specimens were recorded during the winter (January) and spring (March) of 2022.
Diagnosis
Specimens collected: size 20–56 mm, width 1–6 mm. All have 16 segments. Hesione with dorsal longitudinal brownish bands (Figure 3A); prostomium curved laterally (Figure 3B–C); antennae long, 4–6 times as long as wide (Figure 3D); 2 anterior eyes wider, spaced more than posterior ones (Figure 3D); parapodia with dorsal cirri basally cylindrical, dorsal cirrophore three times as long as wide (Figure 3E); larger acicula blackish (Figure 3E); acicular lobe double, 2 tines short, blunt, upper tine slightly longer than lower one (Figure 3E); neurochaetal blades bidentate, 4–6 times as long as wide (Figure 3F & G); subdistal tooth smaller than distal one, with guards approaching distal tooth (Figure 3F & G); posterior end tapered into a blunt cone; pygidium smooth (Figure 3H–I).
Hesione sicula delle Chiaje, 1830; A, preserved specimen, anterior end to the left; B, anterior region and everted pharynx, dorsal view; C, anterior region and everted pharynx, ventral view; D, prostomium dorsal view showing the antennae; E, left parapodium, anterior view; F and G, neurochaetal blades; H, posterior region, dorsal view; I, posterior region, ventral view.
Remarks
This species is found across a vast area, spanning from the Gulf of Vizcaya to the Northwestern African region, including the Mediterranean Sea, specifically the coasts of Girona (Spain), Marseille (France), Monaco, Naples (Italy), and Rovinj (Croatia). It was first recorded in the Mediterranean Sea in Marseille, as noted in M. Barban's collection (Salazar-Vallejo, Reference Salazar-Vallejo2018). However, records from tropical regions, such as the Gulf of Guinea, cast uncertainty, as specimens discovered there may potentially belong to a separate, distinct species. Typically, this species is located in a variety of mixed bottom habitats, ranging from the intertidal zone to depths of up to 50 m. It shares its habitat with H. pantherina Risso, 1826, in the Mediterranean and adjacent regions, and although they have often been regarded as synonyms, they are clearly distinct species (Salazar-Vallejo, Reference Salazar-Vallejo2018).
Discussion
The record of H. sicula in Amsa Bay, on the Mediterranean coast of Morocco, represents the first documented occurrence of this species along the North African Mediterranean coastlines. This finding also marks a noteworthy addition to the Polychaeta list of Morocco, which now comprises a total of 143 genera and 323 species (Gillet, Reference Gillet2017; Mabrouki et al., Reference Mabrouki, Crocetta and Taybi2021). Furthermore, it contributes to our broader understanding of the distribution of this genus and species within the Mediterranean Sea.
The genus Hesione exhibits a wide distribution, with species found in various ocean basins and regions. This distribution has been a subject of taxonomic debate due to the morphological similarities and differences among species of this genus. Some researchers have suggested the existence of synonyms, further complicating the taxonomy and geographical distribution (Costa et al., Reference Costa, De Assis and Christoffersen2008; Ngamniyom et al., Reference Ngamniyom, Silprasit and Sriyapai2014; Salazar-Vallejo, Reference Salazar-Vallejo2018). Hartman (Reference Hartman1959) catalogued all species and proposed several synonymies, suggesting that some species are widely distributed and that certain names should be considered junior synonyms. Recently, Salazar-Vallejo (Reference Salazar-Vallejo2018) revised the taxonomy of this genus, which now comprises a total of 23 species, and reported that the distribution and taxonomy of Hesione species may not be fully resolved. Some regions, particularly in Western Africa, remain inadequately studied, and further research may reveal additional, yet undiscovered species. Additionally, subtidal and nocturnal sampling methods could potentially uncover new Hesione species in well-studied regions. Taxonomic revisions and comprehensive comparisons of specimens from various regions are essential for a better understanding of the distribution and diversity within Hesione.
The distribution of H. sicula is quite extensive, ranging from the Gulf of Vizcaya to the Northwestern African region, encompassing the entire Mediterranean Sea. Records of this species in more tropical localities, such as the Gulf of Guinea, are met with scepticism, as the specimens found there might belong to another closely related species (Salazar-Vallejo, Reference Salazar-Vallejo2018).
Discovering H. sicula in Amsa Bay is noteworthy for several reasons. Firstly, the finding of this species in Amsa Bay underscores the importance of conducting regular biodiversity surveys and monitoring in coastal areas. These efforts allow researchers and conservationists to gain insights into the presence and distribution of various species, which is crucial for understanding ecosystem dynamics, assessing conservation needs, and preserving biodiversity. Secondly, this discovery expands the known geographical distribution range of both the genus Hesione and the species H. sicula in the Mediterranean Sea. Such range extensions can provide valuable data for scientists studying species' responses to environmental changes, including shifts in water temperature, ocean currents, and habitat availability. Furthermore, the presence of H. sicula in Amsa Bay highlights the potential role of shellfish farms in facilitating the establishment of certain marine species. These farms create artificial habitats that may attract and sustain various marine organisms, sometimes leading to the establishment of non-native species. Understanding the interactions between aquaculture operations and local ecosystems is critical for sustainable management practices and minimizing ecological impacts.
This discovery also serves as a reminder of the rich biodiversity that exists along the Mediterranean coastlines of Morocco, in particular, and the Mediterranean coasts of North Africa, in general. It underscores the need for continued research and conservation efforts to protect these unique and often fragile ecosystems. Monitoring changes in species distributions, such as the appearance of H. sicula, can provide valuable insights into how these ecosystems are responding to environmental and anthropogenic pressures.
Conclusion
The first record of H. sicula in Amsa Bay, on the western Moroccan Mediterranean coast, is a noteworthy addition to the Polychaeta list of the North African Mediterranean coasts, and an extension of the geographical distribution range of both the genus and species within the Mediterranean Sea. This finding underscores the imperative for supporting and diversifying research programmes, including monitoring, and conservation initiatives in coastal zones to enhance our comprehension of and safeguard marine biodiversity in response to environmental changes.
Acknowledgments
The authors express their gratitude to the Higher School of Technology of Khénifra (Sultan Moulay Slimane University) and the Polydisciplinary Faculty of Larache (Abdelmalek Essaâdi University – Tetouan) for their academic support. Special thanks are extended to the Amsa Shellfish Research Station (National Institute of Fisheries Research INRH, Tetouan) for providing the necessary technical facilities for conducting the experiments, and to their institutional staff for their invaluable technical assistance. H.J. acknowledges the support of the Moroccan Ministry of Higher Education, Scientific Research, and Innovation through a CNRST (Centre National pour la Recherche Scientifique et Technique) Excellence Research Scholarship grant (#19UAE 2022 (2022–2024)). The authors are also grateful to Professor Sergio Ignacio Salazar Vallejo, from El Colegio de la Frontera Sur, Chetumal, Quintana Roo (Mexico), for his guidance and assistance regarding the systematic classification of the Hesione genus, as well as for his insightful comments and suggestions on an earlier version of the manuscript. Finally, sincere appreciation is extended to Professors Mohamed Ghamizi and Mohamed Cheggour, from Cadi Ayyad University, for their kindness and assistance during the deposition of specimens at the Natural History Museum, Marrakech.
Authors’ contributions
Nor-eddine Chouikh contributed to conceptualization, systematic identification of the species, preparation of Figures 1, 2 and 3, writing the original draft, and reviewing and editing the manuscript. Hafsa Janah and Yassine Ouagajjou conducted the sampling and the extraction process of macrofauna and participated in the preparation of Figures 2 and 3. Adil Aghzar contributed to reviewing and editing the manuscript. All authors reviewed and approved the manuscript.
Financial support
This research received no specific grant from any funding agency, commercial, or not-for-profit sectors.
Competing interests
None.
Data availability
All the data are available upon request.
